Wing bone laminarity is not an adaptation for torsional resistance in bats.

Lee AH, Simons EL - PeerJ (2015)

Bottom Line:
Our results show that humeri from bats across a wide phylogenetic and body size range do not contain any laminar bone.Phylogenetically-informed scaling analyses reveal that the difference in vascularity between birds and bats is best explained by higher somatic relative growth rates in birds.The presence of wing bone laminarity in birds and its absence in bats suggests that laminar bone is not a necessary biomechanical feature in flying vertebrates and may be apomorphic to birds.

ABSTRACTTorsional loading is a common feature of skeletal biomechanics during vertebrate flight. The importance of resisting torsional loads is best illustrated by the convergence of wing bone structure (e.g., long with thin walls) across extant bats and birds. Whether or not such a convergence occurs at the microstructural level is less clear. In volant birds, the humeri and ulnae often contain abundant laminar bony tissue in which primary circumferential vascular canals course concentrically about the long axis of the bone. These circumferential canals and the matrix surrounding them presumably function to resist the tissue-level shear stress caused by flight-induced torsion. Here, we assess whether or not laminar bone is a general adaptive feature in extant flying vertebrates using a histological analysis of bat bones. We sampled the humeri from six adult taxa representing a broad phylogenetic and body size range (6-1,000 g). Transverse thick sections were prepared from the midshaft of each humerus. Bone tissue was classified based on the predominant orientation of primary vascular canals. Our results show that humeri from bats across a wide phylogenetic and body size range do not contain any laminar bone. Instead, humeri are essentially avascular in bats below about 100 g and are poorly vascularized with occasional longitudinal to slightly radial canals in large bats. In contrast, humeri from birds across a comparable size range (40-1,000 g) are highly vascularized with a wide range in bone laminarity. Phylogenetically-informed scaling analyses reveal that the difference in vascularity between birds and bats is best explained by higher somatic relative growth rates in birds. The presence of wing bone laminarity in birds and its absence in bats suggests that laminar bone is not a necessary biomechanical feature in flying vertebrates and may be apomorphic to birds.

Mentions:
The biomechanical influence of flapping flight may also govern organization at the histological level. One of the histological features of bone under investigation is the network of primary vascular canals, which are small channels containing blood vessels, loose connective tissue, and visceral nerves (Ross & Pawlina, 2011). Primary vascular canals vary in orientation across the adult limb skeleton (Fig. 1) and are well-documented particularly in birds (e.g., de Margerie, 2002; de Margerie, Cubo & Castanet, 2002; Skedros & Hunt, 2004; de Margerie et al., 2005; Simons & O’Connor, 2012). In particular, primary vascular canals oriented circumferentially to form laminar bone (Fig. 1A) are abundant in the midshaft humerus. Because this location is hypothesized to experience elevated torsional loading during flight, the presence of laminar bone in the humerus may relate to a biomechanical function (de Margerie, 2002; de Margerie et al., 2005). Wing shape may also influence the proportion of laminar bone in the humerus (laminarity index sensude Margerie, 2002) presumably because broad wings produce greater twisting moments (torques) than narrow wings (de Margerie et al., 2005; Simons & O’Connor, 2012). Together, these findings suggest that laminar bony tissue may be a biomechanical adaptation to flight-induced torsional loads at least in birds (de Margerie, 2002; de Margerie et al., 2005).

Bottom Line:
Our results show that humeri from bats across a wide phylogenetic and body size range do not contain any laminar bone.Phylogenetically-informed scaling analyses reveal that the difference in vascularity between birds and bats is best explained by higher somatic relative growth rates in birds.The presence of wing bone laminarity in birds and its absence in bats suggests that laminar bone is not a necessary biomechanical feature in flying vertebrates and may be apomorphic to birds.

ABSTRACTTorsional loading is a common feature of skeletal biomechanics during vertebrate flight. The importance of resisting torsional loads is best illustrated by the convergence of wing bone structure (e.g., long with thin walls) across extant bats and birds. Whether or not such a convergence occurs at the microstructural level is less clear. In volant birds, the humeri and ulnae often contain abundant laminar bony tissue in which primary circumferential vascular canals course concentrically about the long axis of the bone. These circumferential canals and the matrix surrounding them presumably function to resist the tissue-level shear stress caused by flight-induced torsion. Here, we assess whether or not laminar bone is a general adaptive feature in extant flying vertebrates using a histological analysis of bat bones. We sampled the humeri from six adult taxa representing a broad phylogenetic and body size range (6-1,000 g). Transverse thick sections were prepared from the midshaft of each humerus. Bone tissue was classified based on the predominant orientation of primary vascular canals. Our results show that humeri from bats across a wide phylogenetic and body size range do not contain any laminar bone. Instead, humeri are essentially avascular in bats below about 100 g and are poorly vascularized with occasional longitudinal to slightly radial canals in large bats. In contrast, humeri from birds across a comparable size range (40-1,000 g) are highly vascularized with a wide range in bone laminarity. Phylogenetically-informed scaling analyses reveal that the difference in vascularity between birds and bats is best explained by higher somatic relative growth rates in birds. The presence of wing bone laminarity in birds and its absence in bats suggests that laminar bone is not a necessary biomechanical feature in flying vertebrates and may be apomorphic to birds.